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Hemorrhagic stroke
Original research
Combined standard bypass and parent artery occlusion for management of giant and complex internal carotid artery aneurysms
  1. Philippe Dodier1,
  2. Wei-Te Wang1,
  3. Arthur Hosmann1,
  4. Dorian Hirschmann1,
  5. Wolfgang Marik2,
  6. Josa M Frischer1,
  7. Andreas Gruber3,
  8. Karl Rössler1,
  9. Gerhard Bavinzski1
  1. 1 Department of Neurosurgery, Medical University of Vienna, Wien, Austria
  2. 2 Department of Radiology, Medical University of Vienna, Wien, Austria
  3. 3 Department of Neurosurgery, Kepler Universitätsklinikum GmbH, Linz, Oberösterreich, Austria
  1. Correspondence to Professor Gerhard Bavinzski, Department of Neurosurgery, Medical University of Vienna, Wien 1090, Austria; gerhard.bavinzski{at}meduniwien.ac.at

Abstract

Background Complex aneurysms do not have a standard protocol for treatment. In this study, we investigate the safety and efficacy of microsurgical revascularization combined with parent artery occlusion (PAO) in giant and complex internal carotid artery (ICA) aneurysms.

Methods Between 1998 and 2017, 41 patients with 47 giant and complex ICA aneurysms were treated by an a priori planned combined treatment strategy. Clinical and radiological outcomes were stratified according to mRS and Raymond classification. Bypass patency was assessed. Median follow-up time was 3.9 years.

Results After successful STA–MCA bypass, staged endovascular (n=37) or surgical (n=1) PAO was executed in 38 patients following a negative balloon occlusion test. Intolerance to PAO led to stent/coil treatments in two patients. Perioperative bypass patency was confirmed in 100% of completed STA–MCA bypass procedures. Long-term overall bypass patency rate was 99%. Raymond 1 occlusion and good outcome were achieved in 95% and 97% (mRS 0–2) of cases, respectively. No procedure-related mortality was encountered. Eighty-four percent of patients with preoperative cranial nerve compression syndromes improved during follow-up.

Conclusions The combined approach of STA-MCA bypass surgery followed by parent artery occlusion achieves high aneurysm occlusion and low morbidity rates in the management of giant and complex ICA aneurysms. This combined indirect approach represents a viable alternative to flow diversion in patients with cranial nerve compression syndromes or matricidal aneurysms, and may serve as a backup strategy in cases of peri-interventional complications or lack of suitable endovascular access.

  • aneurysm
  • balloon
  • technique
  • cranial nerve
  • intervention

Data availability statement

All data relevant to the study are included in the article or uploaded as supplementary information. Individual de-identified participant data will not be shared due to the general Data Protection regulation which came into effect on May 25 2018 in Austria. The study protocol in the German language will be available on request.

http://dx.doi.org/10.1136/neurintsurg-2021-017673

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    Introduction

    The grave natural history of giant and complex aneurysms, with reported 5-year rupture rates of up to 50%, necessitates an effective form of therapy.1 Microsurgical clipping as the gold standard allows preservation of the parent artery. However, feasibility of this therapy depends on aneurysm location and factors such as wall calcification, intraluminal thrombus, and involvement of important vessels. Combined surgical morbidity and mortality for complex aneurysms are not negligible and may range from 10% to 45%.1–3

    Hunterian ligation had been introduced as an alternative treatment for otherwise unclippable aneurysms. In selected cases, this technique was supported by microsurgical revascularization to protect the depending vascular territory from ischemia.2–6 With the refinement of endovascular therapy (EVT), combining both methods was regarded as a logical progression, especially by endovascular and hybrid neurosurgeons.5–10 A growing body of evidence supports their preferential use of high-flow grafts.2 11 Few centers only opt to proceed with the “low-flow” bypass technique prior to parent artery occlusion (PAO).12

    We reviewed our experience with standard superficial temporal artery–middle cerebral artery (STA–MCA) revascularization combined with predominantly endovascular PAO in the management of complex internal carotid artery (ICA) aneurysms. To the best of our knowledge, this series represents one of the largest cohort of patients treated in such a way to date.

    Patients and methods

    Study cohort

    Between 1998 and 2017, 2779 aneurysms were treated at our neurosurgical department. Medical records and imaging data were retrospectively analyzed. The study population included patients with giant and complex ICA aneurysms with an a priori planned deconstructive strategy of combined standard STA–MCA revascularization and PAO. Inclusion criteria were age above 18 years and no subarachnoid hemorrhage within 60 days prior to treatment. After exclusion of treatments involving pure endovascular PAO, surgical clipping, and high-flow bypasses, 41 patients harboring 47 complex ICA aneurysms were included in the study (table 1 and online supplemental table 1).

    View this table:
    Table 1

    Baseline characteristics of target aneurysm

    Due to the retrospective study design, the need for informed consent was waived. The study was approved by our institutional ethical review committee. The reporting adheres to the STROBE statement.

    Aneurysm characteristics and indications

    Complex aneurysms were defined as unclippable or difficult to clip after reviewing imaging data according to the following criteria: location, neck dimension, extension into the cavernous sinus, fusiform parent artery configuration, excessive wall calcification, intra-luminal thrombus formation, and/or previous coil treatment.8 In line with the pertinent literature, our institutional selection criteria for the combined indirect treatment have been modified over the past two decades (online supplemental table 2).2 13–19

    Multimodal treatment and BTO technique

    Our bypass technique has been established for several decades and has been slightly modified since its introduction.9 We recently reported on an improved planning workflow for EC-IC revascularization combined with transdural indocyanine green videoangiography (tICG-VA).20 Moreover, online supplemental figure 1 provides a step-by-step description of our institutional double-barrel bypass technique. Intraoperative heparinization was not performed except in one patient with repeated intraoperative donor occlusion. Continuous monitoring was achieved by electroencephalography and somatosensory evoked potential tests in all patients.6 7

    Bypass patency was confirmed intraoperatively by micro-Doppler ultrasonography, indocyanine green video-angiography (since 2007), and ultrasonic flow probe (Transonic Systems Inc., since 2014).7 Intraoperative digital subtraction angiography (DSA) was performed exceptionally.

    After surgery, patients were closely monitored in our ICU, with blood pressure maintained at normotension. Neither heparin nor aspirin was used except for the administration of low-dose heparin to prevent deep venous thrombosis. Due to the anticipated heparinization during planned endovascular PAO, a dry operative field was considered critical throughout surgery.

    Staged, predominantly endovascular PAO was performed at a biplane flat-panel angiographic suite (Axiom Artis, Siemens), usually 48–72 hours after surgery. Generally, patients were embolized under local anesthesia without sedation under anesthesiologic monitoring.

    Prior to PAO, a balloon test occlusion (BTO) of the diseased ICA was performed. The venous phase BTO technique has been traditionally applied at our center since the 1990s as initially described by Vasquez-Anon.21 As the endovascular technique and materials evolved over time, our set-up was adapted to meet the internationally accepted standard operating procedures.22 A balloon catheter (Magic B1, Balt; Hyperglide, Medtronic; or Scepter XC balloon, Microvention) was positioned in coaxial fashion via a guiding catheter (Envoy or Vista Brite; Cordis) proximally adjacent to the aneurysm. Prior to balloon inflation, 4000–5000 IU of heparin (bodyweight-dependent) was administered. Contrast medium injection confirmed sufficient inflation and flow arrest. Patients were continuously monitored and tested for a total duration of 25–30 min with simple motor and language tasks and examined for neurocognitive impairment. If a hypotensive challenge test was deemed necessary, a decrease in systolic blood pressure of approximately 20 mmHg was targeted for a short duration of time (5 min).23 24 Once stable neurology was documented, loose coiling of the aneurysm sac and endovascular PAO were performed with detachable balloons, coils, or a combination of both. Recently, flow-blocking vascular plugs were also placed (UNO, neurovascular embolization system, Reverse Medical) below the petrous ICA after coiling the diseased segment. In the ICU, heparin was continued for 24 hours (aPTT of 60–80 s). Blood pressure was titrated to the desired level and hemodynamics optimized.10 15

    Outcome assessment

    Immediate bypass patency and aneurysm occlusion grades were determined postoperatively by DSA. Radiological follow-up was routinely performed at 6–12 months. The post-treatment MR protocol for investigation for delayed silent infarctions or signal abnormalities due to chronic hypoperfusion, thromboembolic stroke, or perforator stroke consisted of T2, proton-density-weighted spin-echo, and FLAIR sequences. A neuroradiologist and a neurosurgeon evaluated all imaging data blinded to the results. Aneurysm occlusion was assessed according to the Raymond classification.25 Baseline and follow-up neurological data were rated according to the modified Rankin Scale (mRS). We performed an official death-register comparison. Complications were evaluated postoperatively, post-interventionally, and at follow-up. Procedure-related morbidity was defined as any permanent deficit related to treatment (mRS >2). Severe adverse events were defined as major ischemic or hemorrhagic stroke leading to significant neurological deficits (mRS >3). Temporary neurological deficits that resolved completely by discharge or final follow-up were regarded as minor adverse events. Wound-healing problems and non-neurological adverse effects were also documented. Median follow-up time was 3.9 years (range: 0.3–14.8) with a total observation period of 263.7 years.

    Statistical analysis

    Statistical calculations were performed using descriptive analyses, including median and range and total number and percentage. The Mann-Whitney U test and Fishers' exact test were used to assess the differences between the successful BTO and failed BTO groups of patients. Clinical outcome was evaluated by the Wilcoxon test for paired samples. Two-sided P-values<0.05 were considered statistically significant. SPSS Statistics (Version 25.0, IBM Corp.) was used for data administration and statistical calculations.

    Results

    Aneurysm characteristics and indications

    Our study comprised 41 patients with 47 giant or complex ICA aneurysms, which were not amenable to conventional treatments. Aneurysm characteristics are detailed in table 1. Fusiform and dysplastic configurations were seen in 21 patients (21/41, 51%). A total of 90% of target aneurysms were large or giant in size (37/41). Infraclinoidal neck extension was noticed in 15 patients. Indications for indirect combined treatment for complex ICA aneurysms included failed prior coiling attempts (8/41, 20%), lack of endovascular access due to tortuous vascular anatomy (9/41, 22%), and symptomatic patients with cranial nerve (CN) compression syndromes demanding a deconstructive procedure to rapidly diminish mass effect (24/41, 58%).

    Surgical results

    Of the 41 intended STA–MCA bypass surgeries, one procedure (1/41, 2%) was aborted due to thrombosis of the donor vessel, possibly related to vessel injury during preparation. In the remaining 40 cases, a double-barrel STA–MCA bypass was constructed in the majority of cases (33/40, 83%). Median temporary occlusion time of the recipient artery was 30 min (range: 10–45 min). Micro-Doppler ultrasound, indocyanine green video-angiography, or DSA confirmed intraoperative patency in 100% of completed procedures.

    BTO was performed in a median of 2 days (range: 1–57 days) after bypass in 36 patients (36/40, 90%). Of these, BTO was well tolerated by 89% of patients (32/36) and was followed by permanent ICA occlusion. Four patients (4/36, 11%) developed neurological symptoms and BTO was immediately aborted in the first attempt (figure 1). In two of them, the ICA was successfully occluded after negative BTO at a second attempt, 24 hours and 21 days later. PAO without BTO was successfully performed under general anesthesia in the remaining four patients with luxuriant bypass flow (4/40, 10%). In three of them, occlusion was achieved by endovascular means, and in one, surgically (Hunterian clip ligation, 1/40, 2%), due to difficult vascular access. PAO was performed by EVT in all other cases (37/40, 92%). Hence, a combined treatment was executed, as planned, in 38 patients (38/40, 95%). In the remaining two patients, successful EVT with a stent/coil construct was used after poor bypass filling in one and after speech arrest during BTO in another.

    Figure 1
    Figure 1

    Treatment protocol and long-term (≥1 year) follow-up status of 41 patients with 47 complex ICA aneurysms. One procedure (1/41, 2%) was aborted due to thrombosis of the donor vessel during anastomosis. The patient was later treated by stent-assisted coil embolization and was not included in the outcome analysis. 38/40 patients underwent successful PAO. In 2/36 patients (6%), successful stent-assisted coiling was performed later due to failed BTO. Clinical and radiological parameters were available for all patients at baseline and for 37 of the 38 patients (97%) at last follow-up.

    Overall, information regarding bypass patency was available for 39 patients at the last follow-up, including both failed BTO cases with subsequent treatment modification. Patency was confirmed in 92% of patients (36/39) or 93% of all anastomoses (66/71). Notably, initial bypass patency of the failed BTO patients had been demonstrated angiographically before abort of the PAO procedure. However, a significant difference was found in long-term patency rates between the successful and failed first-attempt BTO groups at the last follow-up (P=0.029, n=35). Of the patients who had completed bypass surgery and successful PAO, long-term follow-up was available for 37 patients (figure 1). The patency rate in this group was 99% (66/67 bypass grafts in 36/37 patients) at last follow-up.

    Long-term aneurysm occlusion

    Long-term (≥1 year) aneurysm obliteration rates were available for 37 patients (figure 1). Complete occlusion (Raymond I) was documented in 95% of patients (35/37) at the last follow-up (figure 2). Residual filling was evident on control-angiography in two patients only (2/37, 5%). In one patient (1/37, 3%) a recanalized ICA was diagnosed 2 months after PAO. Retreatment by surgical ICA ligation led to total aneurysm obliteration. Hence, the efficacy of a combined strategy for giant or complex ICA aneurysms was evident with a first-attempt success rate of 89% (33/37 patients, Raymond I). It rose to 95% after retreatment and at the last follow-up. No aneurysmal ruptures were observed during the follow-up period.

    Figure 2
    Figure 2

    Three-dimensional-digital subtraction angiography image of a patient in their 40s complaining of headaches and right-sided progressive impairment of visual acuity caused by a right-sided supraclinoidal fusiform aneurysm (A). Insert shows coil-occluded internal carotid artery aneurysm. Vision recovered completely within 7 months. (B) robust bypass filling of the right middle cerebral artery territory (anteroposterior and lateral view). (C) cross flow from the left side. (D). follow-up MRI demonstrating the thrombosed aneurysm.

    Clinical outcome and complications

    At last follow-up, 97% of patients (36/37) presented with excellent or good clinical outcomes (median mRS: 0, range: 0–2). A statistically significant improvement compared with their preoperative status (median mRS 2) was clinically evident (P<0.001). In one patient, poor outcome was attributed to watershed infarction and postoperative hemiparesis further complicated by severe cardiac disease (table 2). At last follow-up, a complete remission of CN compression syndromes was documented in 10 patients and a marked improvement in a further 10 patients. Thus, 84% (20/24) of patients with CN symptoms responded well to the deconstructive strategy. In four patients (4/24 patients, 16%) symptoms remained unchanged.

    View this table:
    Table 2

    Summary of peri-operative and delayed complications

    At last follow-up, we observed two non-procedure-related deaths 2.7 and 4.9 years after flow replacement surgery (in the first case due to oncological progression of a bronchial carcinoma and in the second due to a traumatic acute subdural hematoma).

    Discussion

    We analyzed one of the largest patient series to date of complex ICA aneurysms, otherwise not amenable to conventional reconstructive methods, who were thus managed by combined microsurgical and endovascular treatment.5 12 Our cohort comprised 41 patients with 47 complex ICA aneurysms with 90% being large or giant in size. Fifteen aneurysms showed infraclinoidal neck extension into the cavernous sinus. All but one patient were treated by standard STA–MCA bypass surgery followed by staged endovascular PAO. With a 99% long-term bypass patency rate, 95% complete aneurysm occlusion, and 97% excellent and good clinical outcome at last follow-up, our results were well within the range reported by other groups.8 12 Careful patient selection may be one of the leading factors resulting in the overall good outcome in this series.

    Patient selection and evolution of the concept

    Before 1996, every patient harboring an unclippable or uncoilable ICA aneurysm was evaluated by a BTO protocol that relied purely on clinical and angiographic testing, including a hypotensive challenge test.13 Although our BTO protocol had low complication rates, we were at an early stage aware of patients developing delayed ischemic symptoms due to hemispheric hypoperfusion the day following successful testing and uneventful PAO.6 10 13–15 In fact, the introduction of a cumbersome and expensive cerebral perfusion assessment protocol using Xenon-enhanced CT during testing could not adequately predict the risk of stroke after ICA sacrifice. Several patients classified as low risk according to their cerebral bloodflow state during BTO still suffered strokes after PAO.6 12–15 Since up to 22% of patients experienced ischemic symptoms after uneventful BTO and completed PAO, pointing toward a high rate of false-negative test results, our institutional workflow was consequently modified.13–15 Moreover, de-novo aneurysm formation or enlargement of preexisting contralateral aneurysms after sole PAO have been frequently reported and also observed by the senior authors.10 13 To detect these potential long-term sequelae, our neuroradiological follow-up recommendations include a MRA follow-up after 6 and DSA after 12 months. After confirmed aneurysm occlusion and bypass patency, further radiological follow-up including MRA is recommended every 3–5 years.

    Currently, only those patients meeting strict criteria undergo BTO directly in our institution. Patients with robust collaterals including well-developed AComA and A1-segments or PComA – as seen on CTA and evaluated by manual compression of the involved ICA during angiography – are now regarded as having the anatomical prerequisites for PAO alone. Chen et al reported 11 cases where failed clinical BTO were associated with absent or hypoplastic AComA and A1-segments.13 Their overall infarction rate after PAO was 20%, probably due to paradoxical blood pressure elevation during BTO. Individual patient characteristics such as age, comorbidities, multiple aneurysms, and additional steno-occlusive diseases are now integrated into our decision process as well.13 All patients who are found likely to develop ischemic symptoms according to published criteria will receive STA–MCA bypass surgery before BTO and PAO.13 15 26

    Since the introduction of Hunterian ligation, treatment modalities and outcomes for these pathologies have changed significantly.4 27 With the development of modern EVT, it became imperative to combine both methods to improve radiological and clinical results.5–7 10 12 The concept seemed especially attractive for dually-trained neurosurgeons.5 10 13 Several publications emphasized the value of integrating modern endovascular techniques with neurosurgical management with the aim of enhancing therapeutic options and reducing technical complication rates.5–7 10 12 15 25 26 28

    In one report on 13 complex ICA aneurysms treated by combined bypass surgery and PAO, complications arose in two patients after high-flow bypass beside thromboembolic events after ICA balloon occlusion.6 The latter was attributed to the technically more demanding balloon occlusion technique, but the resulting 15% complication rate attributed to high-flow bypasses, may question this concept.

    Standard STA–MCA bypass vs high-flow grafts

    Various bypass types have been proposed.2 3 6 9 For years, specialized cerebrovascular units emphasized the application of large grafts (radial artery or saphenous vein) with the intention of substituting entire territories.2 11

    Although high-flow anastomoses have large flow capacities, microsurgery is associated with complication rates reaching 16%.2 11 Even the innovation of non-occlusive techniques, specifically invented to avoid longer occlusion times, could not lower this rate. Van Doormal et al reported a combined mortality and morbidity rate of 16.8% in 34 patients treated non-occlusively.11

    However, studies expressing a balanced view, comparing different revascularization concepts, are limited.12 29 30 Few groups that relied on “low-flow” STA-MCA bypass techniques before PAO reported patency rates up to 99% and low morbidity.5 9 12 29 30 Ponce et al. performed eight STA–MCA bypasses followed by PAO with good clinical outcome.29 Nussbaum et al presented their STA–MCA bypass experience for 30 ICA aneurysms, demonstrating high patency and low complication rates of 98.8% and 4.8%, respectively.12

    Cherian et al described a significantly higher flow rate of up to 120 cc/min when using double-barrel bypasses compared with single-barrel bypasses.30 The observed flow rates match those delivered by radial artery grafts and, thus, question the term “low-flow” bypass. Since the majority of our patients received a double-barrel STA–MCA bypass, Cherian’s findings and our clinical results validate our treatment concept, provided that highest quality standards are followed.30 We summarized our institutional technique and recommendations in online supplemental figure 1. Of note, we encountered 6% (two cases) of wound-healing complications in our long-term follow-up cohort. These complications, while being rare, were only observed among double-barrel cases but were all managed conservatively without long-term sequelae.12

    Our series also includes two patients who failed the initial BTO but went on to be treated successfully by PAO. It may be explained by the ability of grafts to mature and rapidly adapt to the demand by increasing their caliber over short time periods.5 9 30 Consequently, we prefer the term “standard” rather than “low-flow” for double-barrel STA–MCA bypasses.9 12 30

    In our experience, PAO is best performed within 1 week of bypass construction. However, in one patient, endovascular PAO was finalized 57 days after bypass surgery. In contrast to high-flow conduits, requiring immediate performance of PAO, EVT can be postponed and has the advantage of examining the patient while awake during BTO as well as having the opportunity to optimize hemodynamics.6 10 11 25 26 28 29

    Our long-term outcome data are also evidence of the safety and reliability of STA–MCA anastomosis when compared with high-flow conduits.2 11

    Long-term outcomes and comparison with modern endovascular treatment

    EVT techniques evolved at an impressive pace.8 10 31–33 Coil embolization emerged as a treatment of choice for small-necked, saccular aneurysms.31 32 However, large and giant aneurysms demonstrated unsatisfactory long-term results with high recurrences, rebleeding rates of up to 1.9% per year, and M&M rates of 24% and 9%, respectively.33 34

    Our earlier experience with coiling large and giant aneurysms are proof of the challenges surrounding unimodal treatments.33 Later, stent- and balloon-assisted methods resulted in improved radio-anatomical outcomes.7 A recent multicenter analysis reported complete occlusion rates between 67% and 84% after stent-assisted embolization of 670 aneurysms, depending on the used device.35

    Next, flow diverting devices (FDDs) were introduced with the intention of treating giant aneurysms.17 36–40 Short-term safety and efficacy of FDD-induced endoluminal vessel reconstruction with progressive aneurysm occlusion have been demonstrated in several studies, including ours.8 17 36–40 We previously demonstrated complete or near-complete long-term occlusion in 95% cases, comparable to the final PUFS trial occlusion rates that increased from 87% to 95% over time with a retreatment rate of 6% after 5 years.8 40

    Thus, flow diversion undoubtedly represents a major advancement. We also obtained a low-flow diverter-associated complication rate of 5% in a highly preselected cohort.8 A meta-analysis summarizing 1451 patients treated with FDDs reported M&M rates of 5% and 4%, respectively.36 The analysis expressed uncertainty about the safety and risks of FDDs in large and giant aneurysms and did not allow for a clear recommendation. Another important point to be stressed is the complication rate in complex aneurysms after FDD, as addressed by the IntrePED study group.37 They published M&M rates of 13% and 5% for large and 28% and 9% for giant aneurysms, respectively. Notably, the rates for post-operative aneurysm rupture (5, 8%), intraparenchymal hemorrhage (5, 8%), and ischemic stroke (13, 5%) were not negligible, with three of five ruptures occurring in giant aneurysms. In our previous flow diversion series, one of two severe complications arose in a giant lesion.8 In a multicenter study of second-generation FDDs, a potential relationship between size and 30-day mRS was found,

    Impact of modality on cranial nerve compression syndromes

    Patients with CN compressions require longer recovery times after flow diversion due to delayed aneurysmal obliteration and persisting inflow, which may be too long for re-establishing severely compromised visual function.39 While Szikora et al. reported on the improvement of mass effect in most patients presenting with CN deficits (12/16), they also observed visual deterioration after flow diversion.39 Clinical symptoms started to improve as late as 8 months' post-intervention. Another study reported an improvement in 15/28 patients with CN compression.17 In both studies, most patients presented with ophthalmoparesis only and in aneurysms<20 mm in size. Ultimately, both giant aneurysms in the latter study ended up with bypass-supplemented ICA occlusions, since the deployment of six FDDs failed to relieve the mass effect.17 These data suggest that size is definitively a complicating factor for a quick resolution of CN compression, and giant aneurysms more frequently require multiple FDDs to achieve satisfactory occlusion. Both factors might result in critically long recovery times.8 17 39 In contrast, we observed no deterioration in CN function but saw a resolution or marked improvement in 84% of cases (online supplemental figure 1–3). Microsurgical debulking, while principally feasible after PAO but not after FDD due to long-term double antiplatelet therapy, was not necessary to achieve these results.4 5 8 10 12 15 25 26 28 Marked functional improvement occurred by the cessation of arterial pulsations and administration of dexamethasone alone.26 29

    Recently, giant cavernous carotid aneurysms causing external compression and, hence, stenosis of the ICA have been termed “matricidal”. These complex pathologies, associated with CN compression syndromes in 75% of presented cases, are linked with a 30% failed FDD treatment rate. In this study, the authors concluded that parent artery occlusion (with or without bypass) might represent a sound treatment alternative.18

    Consequently, we reason that insecurities concerning FDD as a newer technique remain. A future series of novel endovascular devices should be compared with the reported combined approach herein, which represents an immediate curative approach with an aneurysm obliteration rate of 95% and is associated with low long-term morbidity.

    Limitations, outlook, and conclusion

    The limitations of our study are its retrospective and center-based nature, the relatively small sample size, and the selection of patients based on experience alone. In our opinion, both flow diversion and combined STA–MCA bypass and PAO, are equally safe treatment options in experienced hands. Although the balance has shifted in favor of FDDs recently, our long-term outcome data allow us to carefully select patients and tailor the treatment for each patient.

    Although nowadays more centers are opting for the flow-diversion technique alone, the combined indirect approach represents a viable alternative to flow diversion in patients with cranial nerve compression syndromes or matricidal aneurysms, and may serve as a backup strategy in cases of peri-interventional complications or lack of suitable endovascular access.

    Data availability statement

    All data relevant to the study are included in the article or uploaded as supplementary information. Individual de-identified participant data will not be shared due to the general Data Protection regulation which came into effect on May 25 2018 in Austria. The study protocol in the German language will be available on request.

    Ethics statements

    Patient consent for publication

    Ethics approval

    The study was approved by our institutional ethical review committee (EK No. 1339/2015, 1246/2018).

    Acknowledgments

    The authors appreciate the work of Bernd Richling and Heber Ferraz-Leite contributing to the development of a combined multimodal concept in Vienna. The authors wish to thank the administrative support of Jakob Zagata, Marie-Christine Lunzer, Fabian Winter, and Thomas Haider.

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    Footnotes

    • Presented at Preliminary data were presented at the Annual Meeting of the Austrian Neurosurgical Society 2018 (ÖGNC) and at the Congress of the European Association of Neurosurgical Societies 2019 (EANS).

    • Contributors Conception and design: PD, JMF, GB. Acquisition of data: PD. Analysis and interpretation of data: all authors. Drafting the article: all authors. Critically revising the article: all authors. Study supervision: JMF, KR, GB.

    • Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial, or not-for-profit sectors.

    • Competing interests None declared.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.